Patterns of male fitness conform to predictions of evolutionary models of late life

We studied lifetime male virility, a male fitness component, in five populations of Drosophila melanogaster. Virility was measured as the number of females, of eight total, that a male could fertilize in 24 h. Individual males were measured at weekly intervals until they died. Virility declined in an approximately linear fashion for the first 3 weeks of adult life. It then stayed low but relatively constant for another 3 weeks, exhibiting a clear plateau. These observations are consistent with the evolutionary theories of late life. The results were not consistent with a simple heterogeneity theory of late life. This is the first demonstration of a late-life plateau for a male fitness component. We also found that the virility of males that were within 7 days of death was significantly lower than that of similarly aged males that were not about to die. This rapid deterioration of virility prior to death, or death spiral, is similar to a decline in fecundity that we had previously documented.     

The Impact of male reproductive skew on kin structure and sociality in multi‐male groups

Patterns of within‐group relatedness are expected to affect the prospects for cooperation among group members through kin selection. It has long been established that dispersal patterns determine the availability of kin and there is ample evidence of matrilineal kin biases in social behavior across primate species. However, in 1979, Jeanne Altmann¹ suggested that mating patterns also influence the structure of within‐group relatedness; high male reproductive skew and the frequent replacement of breeding males leads to relatively high levels of paternal relatedness and age‐structured paternal sibships within groups. As a consequence of frequent replacement of breeding males, relatedness among offspring of a given female will be reduced to the half‐ rather than full‐sibling level. Depending on the number of sires and degree of relatedness among mothers, members of the same birth cohort may be as closely related as maternal siblings. If animals are able to recognize their paternal kin and exhibit biases in favor of them, this may influence the distribution of cooperation and the intensity of competition within groups of primates. Here, I summarize the evidence that serves as the basis for Altmann's predictions and review evidence regarding whether or not the availability of paternal kin also leads to paternal kin bias among primates.     

Subadult male orangutan sociality and reproductive behavior at Tanjung Puting

During a four-year period at Tanjung Puting Reserve, Central Indonesian Borneo, subadult males were observed for 670.5 observation hours, 463 hours of which were as focal individuals. Subadult males were quite gregarious, participating in groupings for 40.9% of the time they were observed as targets. Subadult male sociality centered around females; 83% of the time subadult males spent in groupings was exclusively with females, as compared to 3% of contact time spent exclusively with other males. Much subadult male sociality can be understood in terms of male-male competition for females. Interactions between adult and subadult males were almost entirely determined by the presence or absence of females. Adult males were more belligerent when females were present. Twenty-two copulations or attempted copulations occurred during 16 subadult male-female encounters, two of which were consortships. The majority of subadult male copulations (86%) were resisted matings. Outside of consortship, resisted matings (or the first in a series of resisted matings or attempts) usually took place at encounter or shortly thereafter. Subadult males also surreptitiously followed adult males and their consorts. Subadults frequently located receptive females before adult males did but were replaced by adult males when these appeared. Subadult male reproductive strategy consisted of both sneak/“rape” and consort tactics with sneak/“rape” predominating.     

The sociality–health–fitness nexus: synthesis,conclusions and future directions

This theme issue has highlighted the links between sociality, health and fitness in a broad range of organisms, and with approaches that include field and captive studies of animals, comparative and meta-analyses, theoretical modelling and clinical and psychological studies of humans. In this concluding chapter, we synthesize the results of these diverse studies into some of the key concepts discussed in this issue, focusing on risks of infectious disease through social contact, the effects of competition in groups on susceptibility to disease, and the integration of sociality into research on life-history trade-offs. Interestingly, the studies in this issue both support pre-existing hypotheses, and in other ways challenge those hypotheses. We focus on unexpected results, including a lack of association between ectoparasites and fitness and weak results from a meta-analysis of the links between dominance rank and immune function, and place these results in a broader context. We also review relevant topics that were not covered fully in this theme issue, including self-medication and sickness behaviours, society-level defences against infectious disease, sexual selection, evolutionary medicine, implications for conservation biology and selective pressures on parasite traits. We conclude by identifying general open questions to stimulate and guide future research on the links between sociality, health and fitness.     

Maternal effect genes and the evolution of sociality in haplo-diploid organisms

Maternal care and female-biased sex ratios are considered by many to be essential prerequisites for the evolution of eusocial behaviors among the hymenoptera. Using population genetic models, I investigate the evolution of genes that have positive maternal effects but negative, direct effects on offspring fitness. I find that, under many conditions, such genes evolve more easily in haplo-diploids than in diplo-diploids. In fact, the conditions are less restrictive than those of kin selection theory, which postulate genes with negative direct effects but positive sib-social effects. For example, the conditions permitting the evolution of maternal effect genes are not affected if females mate multiply, whereas multiple mating reduces the efficacy of kin selection by reducing genetic relatedness within colonies. Inbreeding also differentially facilitates evolution of maternal effect genes in haplo-diploids relative to diplo-diploids, although it does not differentially affect the evolution of sib-altruism genes. Furthermore, when the direct, deleterious pleiotropic effect is restricted to sons, a maternal effect gene can evolve when the beneficial maternal effect is less than half (with inbreeding, much less) of the deleterious effect on sons. For kin selection, however, the sib-social benefits must always exceed the direct costs because genetic relatedness is always less than or equal to 1.0. The results suggest that haplo-diploidy facilitates (1) the evolution of maternal care, and (2) the evolution of maternal effect genes with antagonistic pleiotropic effects on sons. The latter effect may help explain the tendency toward female-biased sex ratios in haplo-diploids, especially those with inbreeding. I conclude that haplo-diploidy not only facilitates the evolution of sister-sister altruism by kin selection but also facilitates the evolution of maternal care and female-biased sex ratios, two prerequisites for eusociality.     

Blood parasites and male fitness in the pied flycatcher

In vertebrates the effect of parasites on host ecology has almost been ignored. Recently the view that well-adapted parasites do not harm their hosts has been challenged and there is growing evidence that parasites do have a present-day effect on a great variety of host fitness components. The pied flycatcher is a small migratory passcrine bird. Any decrease in condition caused by disease should affect its ability to cope with physical demands of migration. Here we examine whether blood parasites have any effect on male arrival time. Males infected with Trypanosoma arrived on average 2 days later than males with no Trypanosoma infection. Infected males also had shorted tails and tended to have shorter wings. By contrast, there was no difference in male arrival time between males infected with Haemoproteus and healthy males. It seems that Trypanosoma infection lowered male condition and consequently the ability to moult and migrate. The difference in length of feathers may have generated the difference in arrival times. Early arrival is highly important for males, since only the first males become polygynous and breeding prospects deteriorate rapidly with any delay in egg laying. Estimated reduction in breeding success for infected males was about 20%.     

Greeting,aggression, and coalitions between male baboons: Demographic correlates

Interactions of asymmetrical, symmetrical, and unreciprocated greeting, and episodes of aggression and coalitions observed between 18 males, members of a large multi-harem colony of baboons (Papio hamadryas, P. cynocephalus, and their hybrids) housed in the Madrid Zoo, were recorded throughout 11 time blocks between January 1983 and March 1985. The major question investigated was whether the demographic characteristics of the colony affected the frequency with which males used three behavioural strategies, namely, greeting, aggression, and coalitions. It was found that under demographic conditions eliciting more intense male-male competition, for example, when the ratio of oestrous cycles per adult male was lower, males exchanged frequent greetings, especially the symmetrical form (i.e. notifying) and solicited more coalitions, but did not show any significant change in rates of dyadic aggression. Male phenotype-related effects on rates of greeting and coalitions were found as well. Results are discussed in relation with the suggested role of greeting and of coalition behaviour as strategies used in the negotiation of changes in competitive social relationship (e.g. consort changeovers). These strategies are regarded as social tactics alternative to direct aggression.     

Evolution of sociality by natural selection on variances in reproductive fitness: evidence from a social bee

Background  

The Central Limit Theorem (CLT) is a statistical principle that states that as the number of repeated samples from any population increase, the variance among sample means will decrease and means will become more normally distributed. It has been conjectured that the CLT has the potential to provide benefits for group living in some animals via greater predictability in food acquisition, if the number of foraging bouts increases with group size. The potential existence of benefits for group living derived from a purely statistical principle is highly intriguing and it has implications for the origins of sociality.     

Effects of foliar herbivory by insects on the fitness of Raphanus raphanistrum: damage can increase male fitness

Generally, effects of herbivory on plant fitness have been measured in terms of female reproductive success (seed production). However, male plant fitness, defined as the number of seeds sired by pollen, contributes half of the genes to the next generation and is therefore crucial to the evolution of natural plant populations. This is the first study to examine effects of insect herbivory on both male and female plant reproductive success. Through controlled field and greenhouse experiments and genetic paternity analysis, we found that foliar damage by insects caused a range of responses by plants. In one environment, damaged plants had greater success as male parents than undamaged plants. Neither effects on pollen competitive ability nor pollinator visitation patterns could explain the greater siring success of these damaged plants. Success of damaged plants as male parents appeared to be due primarily to changes in allocation to flowers versus seeds after damage. Damaged plants produced more flowers early in the season, but not more seeds, than undamaged plants. Based on total seed production, male fitness measures from the first third of the season, and flower production, we estimated that damaged and undamaged plants had equal total reproductive success at the end of the season in this environment. In a second, richer environment, damaged and undamaged plants had equal male and female plant fitness, and no traits differed significantly between the treatments. Equal total reproductive success may not be ecologically or evolutionarily equivalent if it is achieved differentially through male versus female fitness. Genes from damaged plants dispersed through pollen may escape attack from herbivores, if such attack is correlated spatially from year to year.     

Susceptibility of the male fitness phenotype to spontaneous mutation

Adult reproductive success can account for a large fraction of male fitness, however, we know relatively little about the susceptibility of reproductive traits to mutation-accumulation (MA). Estimates of the mutational rate of decline for adult fitness and its components are controversial in Drosophila melanogaster, and post-copulatory performance has not been examined. We therefore separately measured the consequences of MA for total male reproductive success and its major pre-copulatory and post-copulatory components: mating success and sperm competitive success. We also measured juvenile viability, an important fitness component that has been well studied in MA experiments. MA had strongly deleterious effects on both male viability and adult fitness, but the latter declined at a much greater rate. Mutational pressure on total fitness is thus much greater than would be predicted by viability alone. We also noted a significant and positive correlation between all adult traits and viability in the MA lines, suggesting pleiotropy of mutational effect as required by 'good genes' models of sexual selection.     

Patterns of MHC selection in African mole-rats, family Bathyergidae: the effects of sociality and habitat

African mole-rats are a family of rodents exhibiting an eclectic range of social behaviour and occupying a variety of habitat types. These differences are likely to impact upon the risk of parasite transmission and virulence, with increasing sociality predicted to correspond to an increased risk of transmission. We investigate these factors by analysing the major histocompatibility complex (MHC), a set of genes responsible for encoding highly variable intermediaries of the vertebrate adaptive immune response. To this end we assessed selection at exons 2 and 3 of the MHC class II DQalpha1 gene of four African mole-rat species representing a range of social behaviours. We demonstrate that: (i) the overall pattern of selection at these exons differentiates according to the predicted function of different regions, with the presence of positive selection indicating the likely influence of host-parasite coevolution; and (ii) contrary to the often observed and predicted positive correspondence between sociality and the risk of parasite transmission, two highly social African mole-rat species in fact appear to have comparatively weak positive selection, suggesting diminished host immunity and thus a low overall risk of parasite transmission.     

Inbreeding depression and male fitness in black grouse

The male lifetime lekking performance was studied, and related to inbreeding-outbreeding in a wild population of black grouse (Tetrao tetrix) in central Finland between 1989 and 1995. Inbreeding was measured as the mean heterozygosity and mean d(2) of 15 microsatellite loci. We found a significantly positive relationship between mean d(2) and lifetime copulation success (LCS), while the relationship between heterozygosity and LCS was close to significant. We also found that males that never obtained a lek territory had significantly lower mean heterozygosity than males that were observed on a territory at least during one mating season in their life. Furthermore, among males that were successful in obtaining a lek territory, LCS and mean d(2) were highest for those males that held central territories. We suggest that inbred males have a disadvantage (or outbred males have an advantage) in the competition for territories that may explain the relationships with LCS and inbreeding. Furthermore, the fact that mean d(2) was positively correlated with LCS whereas heterozygosity was not when we restricted the analysis to territorial males, suggests that mean d(2) provides more information about levels of inbreeding-outbreeding than heterozygosity alone, and potentially highlights the effects of heterosis. To our knowledge, this is the first time that measures of inbreeding and lifetime fitness have been linked in a non-isolated population. This is important in establishing that the relationships found in previous studies are not artefacts of low gene flow created by limited dispersal but a general feature of wild vertebrate populations.     

Physical fitness and anthropometrical profile of the Brazilian male judo team

The present study had as objectives (1) to compare the morphological and functional characteristics of the male judo players of the Brazilian Team A (n=7) with the judo players of Teams B and C (reserves; n=15), and (2) to verify the association between the variables measured. Thus, 22 athletes from the seven Olympic weight categories were submitted to: a body composition evaluation (body mass, height, ten skinfolds, eight circumferences, three bone diameters and percent body fat estimation); the Special Judo Fitness Test (SJFT); maximal strength tests (one repetition-maximum, 1 RM, in bench press, row, and squat); and the Cooper test. One-way analysis of covariance was used to compare the groups. The relationships between variables were determined by the Pearson coefficient correlation. The significance level was fixed at 5%. No significant difference was found in any variable between them. The main significant correlations observed were between the following variables: VO2max and number of throws in the SJFT (r=0.79); percent body fat and estimated VO2max (r=-0.83) and number of throws in the SJFT (r=-0.70); chest circumference and bench press 1 RM (r=0.90) and in the row (r=0.80); and thigh circumference and squat 1 RM (r=0.86). However, there was no significant correlation between circumferences and 1 RM/kg of body mass. According to these results the main conclusions are: (1) the physical variables measured do not discriminate performance when analysis is directed to the best athletes; (2) a higher percent body fat is negatively correlated with performance in activities with body mass locomotion (Cooper test and the SJFT); (3) judo players with higher aerobic power performed better in high-intensity intermittent exercise; (4) judo players with bigger circumferences present bigger absolute maximal strength.     

Cross-generational fitness benefits of mating and male seminal fluid

In many species, the physical act of mating and exposure to accessory gland proteins (Acps) in male seminal fluid reduces female survival and offspring production. It is not clear what males gain from harming their sexual partners or why females mate frequently despite being harmed. Using sterile strains of Drosophila melanogaster that differ in their production of Acps, we found that both the physical act of mating and exposure to male seminal fluid in mothers increase the fitness of daughters. We show that the changes in daughter fitness are mediated by parental effects, not by sexual selection involving good genes or owing to variation in maternal egg production. These results support the idea that male harm of females might partly evolve through cross-generational fitness benefits.     

Ectoparasite loads decrease the fitness of alpine marmots (Marmota marmota) but are not a cost of sociality

Parasites arc often considered an unavoidable cost of livingin groups. We examined this hypothesis by investigating theectoparasite fauna of a free-living alpine marmot population,a highly social sciurid species. Only a single important ectoparasitewas found, the mite Echinonyssus blanchardi. Heavy infestationwith this mite correlated with reproductive success of marmotsin two ways. Infant winter mortality increased with ectoparasiteload, probably because ectoparasites reduced the ability ofparents and alloparents to warm infants during hibernation.Litters produced by females exposed to a high number of mitesduring the preceding winter were weaned later. Late weanershad a lower chance of surviving hibernation. However, we foundno relationship between ectoparasite load and group size ormarmot density. Instead, the number of E. blanchardi per animalwas lower in areas where marmot groups were clumped, i.e., infavorable habitats. Although ectoparasites most likely decreasethe fitess of alpine marmots to some extent, they should notbe considered a cost of social life in this species.     

Consequences of genetic incompatibility on fitness and mate choice: the male point of view

Hymenopterans under single‐locus complementary sex determination (sl‐CSD) face inbreeding costs due to this sex determination mode. Under sl‐CSD, homozygote eggs at the sl‐CSD locus usually develop into unviable or sterile diploid males. Production of such costly males increases when sib‐mating happens because related individuals share half of their genome. In the hymenopteran Venturia canescens (a solitary parasitoid wasp), diploid males are sterile, leading to fitness costs through genetic incompatibility between parents. Whereas the costs of producing diploid males and behavioural strategies that would reduce such costs have been studied in females, the potential fitness costs faced by males have not. Here, we aimed to investigate fitness costs that males endure after a single sib‐mating and tested whether they have the ability to avoid sib‐mating through kin recognition. Our results show that males have a reduced fitness (i.e. they produce fewer daughters) when mating with their sibs. We also show that males have the ability to distinguish between non‐sib and sib females (i.e. kin). They use chemical marks emitted by the females to discriminate kin from non‐kin. We discuss the evolution of kin recognition in males in the context of mate choice for genetic compatibility. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 279–286.     

Effect of host size on male fitness in the parasitoid wasp Dinarmus basalis

The effect of host size on male fitness was tested in the parasitoid wasp Dinarmus basalis (Hymenoptera, Pteromalidae) using hosts of different fresh weight. Fitness was measured as the sperm stock in seminal vesicles, and the ability to access females in single or competition situations. Both body size and sperm in seminal vesicles increased with host fresh weight. Males from small hosts had a reduced size and sperm stock compared to those from larger hosts. In single situations, males from both small and large hosts had similar reproductive capacities, whereas in multiple mating or competition situations, males from small hosts were at a disadvantage, inseminating fewer females and copulating less frequently. However, females did not appear to choose between males, and no effect on sperm stored in the spermatheca was observed. Being small does not prevent a D. basalis male mating and producing progeny in single situations, although more offspring could be expected from larger males because of their better competitive abilities.     

Effects on male fitness of removing Wolbachia infections from the mosquito Aedes albopictus

Abstract.  Cytoplasmic incompatibility (CI) induced by maternally inherited Wolbachia bacteria is a potential tool for the suppression of insect pest species with appropriate patterns of infection. The Asian tiger mosquito Aedes albopictus (Skuse) (Diptera: Culicidae) is known to be infected by two strains of Wolbachia pipientis Hertig (Rickettsiales: Rickettsiaceae), w Alb A and w Alb B, throughout its geographical distribution. This infection pattern theoretically restricts the application of CI-based control strategies. However, Wolbachia can be horizontally transferred using embryonic microinjection to generate incompatible transfected lines harbouring a single new strain of Wolbachia. In order to assess the feasibility of this approach, the effects of Wolbachia removal on mosquito fitness need to be clearly evaluated as the removal of natural superinfection is an inescapable step of this approach. Previous research has shown that uninfected females, produced by antibiotic treatment, showed a decrease in fitness compared with those infected with Wolbachia. In this study, the effect of Wolbachia removal on male fitness was investigated. Longevity and reproductive potential (mating competitiveness and sperm capacity) were assessed in both laboratory cages and greenhouses. No differences were observed between uninfected and infected males with respect to longevity, mating rate, sperm capacity and mating competitiveness in either laboratory conditions or greenhouses. The preservation of fitness in males of Ae. albopictus deprived of natural Wolbachia infection is discussed in relation to the development of incompatible insect technique suppression strategies. Finally, the potential application of aposymbiotic males in mark–release–recapture studies is suggested.